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The Potential Roles of Eutrophication and Climate Change Harmful Algae 14 (2012) 313–334 Contents lists available at SciVerse ScienceDirect Harmful Algae jo urnal homepage: www.elsevier.com/locate/hal The rise of harmful cyanobacteria blooms: The potential roles of eutrophication and climate change a, b b c J.M. O’Neil *, T.W. Davis , M.A. Burford , C.J. Gobler a University of Maryland, Center for Environmental Science, Horn Point Laboratory, Cambridge, MD 21613, USA b Griffith University, Australian Rivers Institute, Nathan, QLD 4111, Australia c Stony Brook University, School of Marine and Atmospheric Science, Stony Brook, NY, USA A R T I C L E I N F O A B S T R A C T Article history: Cyanobacteria are the most ancient phytoplankton on the planet and form harmful algal blooms in Available online 29 October 2011 freshwater, estuarine, and marine ecosystems. Recent research suggests that eutrophication and climate change are two processes that may promote the proliferation and expansion of cyanobacterial harmful Keywords: algal blooms. In this review, we specifically examine the relationships between eutrophication, climate Climate change change and representative cyanobacterial genera from freshwater (Microcystis, Anabaena, Cylindros- Cyanobacteria permopsis), estuarine (Nodularia, Aphanizomenon), and marine ecosystems (Lyngbya, Synechococcus, CyanoHABs Trichodesmium). Commonalities among cyanobacterial genera include being highly competitive for low Eutrophication concentrations of inorganic P (DIP) and the ability to acquire organic P compounds. Both diazotrophic (= Harmful algae blooms Toxins nitrogen (N2) fixers) and non-diazotrophic cyanobacteria display great flexibility in the N sources they exploit to form blooms. Hence, while some cyanobacterial blooms are associated with eutrophication, several form blooms when concentrations of inorganic N and P are low. Cyanobacteria dominate phytoplankton assemblages under higher temperatures due to both physiological (e.g. more rapid growth) and physical factors (e.g. enhanced stratification), with individual species showing different temperature optima. Significantly less is known regarding how increasing carbon dioxide (CO2) concentrations will affect cyanobacteria, although some evidence suggests several genera of cyanobacteria are well-suited to bloom under low concentrations of CO2. While the interactive effects of future eutrophication and climate change on harmful cyanobacterial blooms are complex, much of the current knowledge suggests these processes are likely to enhance the magnitude and frequency of these events. ß 2011 Elsevier B.V. All rights reserved. 1. Introduction harmful cyanobacterial blooms have included increased nutrient inputs, the transport of cells or cysts via anthropogenic activities, While cyanobacterial harmful algal blooms have been reported and increased aquaculture production and/or overfishing that in the scientific literature for more than 130 years (Francis, 1878), alters food webs and may permit harmful species to dominate algal in recent decades, the incidence and intensity of these blooms, as communities (GEOHAB, 2001; HARRNESS, 2005; Heisler et al., well as economic loss associated with these events has increased in 2008). It has also been shown that an increase in surface water both fresh and marine waters (Chorus and Bartram, 1999; temperatures due to changing global climate could play a role in Carmichael, 2001, 2008; Hudnell, 2008; Heisler et al., 2008; the proliferation of cyanobacterial blooms (Peperzak, 2003; Paerl Hoagland et al., 2002; Paerl, 2008; Paul, 2008; Paerl and Huisman, and Huisman, 2008; Paul, 2008). Importantly, there is consensus 2008). Recently, there have been discoveries of previously that harmful algal blooms are complex events, typically not caused unidentified cyanobacterial toxins, such as amino b-methyla- by a single environmental driver but rather multiple factors mino-L-alanine (BMAA), and of new genera of cyanobacteria occurring simultaneously (Heisler et al., 2008). Finally, an capable of producing previously described toxins (Cox et al., 2003, improved ability to detect and monitor harmful cyanobacterial 2005, 2009; Cox, 2009; Brand, 2009; Kerbrat et al., 2011). To date, blooms, and their toxins as well as increased scientific and public factors identified as contributing towards the global expansion of awareness of these events has also led to better documentation of these events (GEOHAB, 2001; HARRNESS, 2005; Sivonen and Bo¨rner, 2008). There have been several reviews of the intensification and * Corresponding author. E-mail address: [email protected] (J.M. O’Neil). global expansion of harmful cyanobacterial blooms in terms of 1568-9883/$ – see front matter ß 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.hal.2011.10.027 314 J.M. O’Neil et al. / Harmful Algae 14 (2012) 313–334 both abundance, geographic extent, and effects on ecosystem in the Baltic Sea, an ecosystem whose primary production is health, as well as factors that may be facilitating this expansion dominated by cyanobacteria, BMAA has been measured in (Paerl, 1988, 1997; Paerl and Millie, 1996; Soranno, 1997; significant quantities in both fish and shellfish (Jonasson et al., Carmichael, 2001; Saker and Griffiths, 2001; Landsberg, 2002; 2010). Codd et al., 2005a,b; Huisman and Hulot, 2005; see multiple papers in Hudnell, 2008). The purpose of this review is to: (1) Highlight 2.2. Nutrients important findings of the last decade of harmful cyanobacterial bloom research in fresh, estuarine and marine environments; and Of all of the potential environmental drivers behind harmful (2) Describe how factors associated with eutrophication and algal and cyanobacterial blooms, the one that has received the climate change affect some of the most widely studied harmful most attention among the global scientific community has been cyanobacterial bloom genera. anthropogenic nutrient pollution. Research indicates that cultural eutrophication associated with the increased global human 2. Background population has stimulated the occurrences of harmful algal blooms (Anderson, 1989; Hallegraeff, 1993; Burkholder, 1998; Anderson Cyanobacteria are prokaryotes but have historically been et al., 2002; Glibert et al., 2005; Glibert and Burkholder, 2006; grouped with eukaryotic ‘‘algae’’ and at varying times have been Heisler et al., 2008). As bodies of freshwater become enriched in referred to as: blue–greens, blue–green algae, Myxophyceae, nutrients, especially phosphorus (P), there is often a shift in the Cyanophyceae and Cyanophyta (Carmichael, 2008). More recently phytoplankton community towards dominance by cyanobacteria cyanobacteria that form harmful blooms have been termed (Smith, 1986; Trimbee and Prepas, 1987; Watson et al., 1997; Paerl ‘‘CyanoHABs’’ (Carmichael, 2001, 2008; Paerl, 2008) or ‘‘cyano- and Huisman, 2009). Examples of these changes are the dense bacterial blooms’’ (Hudnell et al., 2008). blooms often found in newly eutrophied lakes, reservoirs, and rivers previously devoid of these events (Fogg, 1969; Reynolds and 2.1. Toxins Walsby, 1975; Reynolds, 1987; Paerl, 1988, 1997). Empirical models predict that in temperate ecosystems, summer phyto- Many genera of cyanobacteria are known to produce a wide plankton communities will be potentially dominated by cyano- variety of toxins and bioactive compounds, which are secondary bacteria at total phosphorus (TP) concentrations of 100– À1 metabolites (i.e. compounds not essential to the cyanobacteria for 1000 mg L (Trimbee and Prepas, 1987; Jensen et al., 1994; growth or its own metabolism) (Sivonen and Jones, 1999). Toxins Watson et al., 1997; Downing et al., 2001). generally refer to compounds that cause animal and human One reason that P often controls the proliferation of freshwater poisonings or health risks, and bioactive compounds refer to ecosystems is that many cyanobacteria that bloom in warm waters compounds that can have antimicrobial and cytotoxic properties have the ability to fix nitrogen (N; Paerl, 1988; Paerl et al., 2001). and are often of interest in pharmaceutical and as research tools Since many of the bloom forming cyanobacteria genera are not (Codd et al., 2005a,b). While many of these compounds have diazotrophic and the proliferation of some blooms may be limited recognized toxic effects, the impact and long term effects of many by N (Gobler et al., 2007; Davis et al., 2010), it has been of these compounds is unknown (Tonk, 2007). hypothesized both N and P may control harmful cyanobacterial Hepatotoxins are globally the most prevalent cyanobacterial blooms (Paerl et al., 2008; Paerl and Huisman, 2009). While toxins followed by neurotoxins (Sivonen and Jones, 1999; Klisch research on cyanobacterial blooms has traditionally considered and Ha¨der, 2008; Sivonen and Bo¨rner, 2008). Hepatotoxins inorganic N and P pools as being accessed by cyanobacteria or total include: (1) microcystins, (2) nodularins, and (3) cylindrosper- N and P pools for understanding the trophic state of ecosystems, mopsins. The three most commonly produced types of cyano- recent research has demonstrated that organic N and P may be bacterial neurotoxins are: (1) anatoxin-a, (2) anatoxin-a (S), and important nutrient sources for cyanobacteria. Much of the soluble (3) saxitoxins. As noted above, Cox et al. (2003, 2005) recently N and P pools in most aquatic environments are comprised of described the presence of the neurotoxic compound, BMAA in organic compounds (Franko and Heath, 1979; Seitzinger and nearly all cyanobacteria they tested (Table 1). It has been Sanders,
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